Ghost rodents: Albinism in Australian rodent species

Abstract While almost half of all mammal species are rodents, records of albinism in free‐ranging rodents are very rare. Australia has a large and diverse assemblage of native rodent species, but there are no records of free‐ranging albino rodents in the published literature. In this study, we aim to improve our understanding of the occurrence of albinism in Australian rodent species by collating contemporary and historic records of this condition and providing an estimate of its frequency. We found 23 records of albinism (i.e., a complete loss of pigmentation), representing eight species, in free‐ranging rodents native to Australia, with the frequency of albinism being generally <0.1%. Our findings bring the total number of rodent species in which albinism has been recorded globally to 76. While native Australian species represent only 7.8% of the world's murid rodent diversity, they now account for 42.1% of murid rodent species known to exhibit albinism. We also identified multiple concurrent albino records from a small island population of rakali (Hydromys chrysogaster) and discuss the factors that may contribute to the relatively high frequency (2%) of the condition on this island. We suggest that the small number of native albino rodents recorded in mainland Australia over the last 100 years means that traits associated with the condition are likely deleterious within populations and are thus selected against.

, but unlike true albinism, it rarely affects skin and does not affect the eyes (Miller, 2005;van Grouw, 2006).
Albinism is rare and typically affects one in several thousand individuals (Fernández et al., 2021). It is generally (though not always, e.g., Sage, 1962) passed on via an autosomal recessive inheritance pattern (i.e., offspring must inherit one copy of the recessive gene from both parents), and an elevated frequency of albinism typically reflects low-genetic diversity within a population (Bensch et al., 2000;Holyoak, 1978).
Despite the rarity of the condition, albinism is often associated with rodents. Some Muridae species, particularly the brown rat (also known as the Norway or laboratory rat; Rattus norvegicus), have been selectively bred for albinism for over a century for domestication (e.g., as pets) and research purposes (Beermann et al., 2004;Castle, 1947;Castle & Allen, 1903;Hou & Protopopova, 2022;Modlinska & Pisula, 2020;Noirot, 1966;Novikova & Grigoryan, 2020). However, albinism in free-ranging rodents appears to be uncommon and has been recorded in fewer than 2% of rodent species globally (Nations et al., 2021;Romero et al., 2018).
Australia has a diverse and ubiquitous assemblage of murid rodents that comprised at least 67 species before European invasion (Menkhorst & Knight, 2004;Roycroft et al., 2021; van Dyck & Strahan, 2008). Since that time, however, at least 13 native rodent species have become extinct, and an additional 25 species have declined enough in distribution and abundance to warrant listing as threatened at State or Federal levels (DAWE, 2021;DELWP, 2021;Northern Territory Government, 2021;OEH, 2021;South Australian Government, 2021). Four invasive rodent species also occur in the country: the brown rat, black rat (R. rattus), pacific rat (R. exulans), and house mouse (Mus musculus; Menkhorst & Knight, 2004;van Dyck & Strahan, 2008). Despite the ubiquity of rodents in Australia, to our knowledge, there are no records of native albino rodents in the published literature (Romero et al., 2018). In the gray literature, however, there is a recent mention of albinism in a population of rakali (Hydromys chrysogaster) on Barrow Island, Western Australia, with multiple albino rakali sightings on the island in recent years (Bettink, 2016). Barrow Island (202 km 2 ) is located 90 km northeast of Onslow and represents a taxonomically distinct population that is typically smaller with lighter pelage compared to populations on the Australian mainland (Bettink, 2016).
In this study, we aim to improve our understanding of the occurrence of complete or true albinism (i.e., a total loss of pigmentation) in Australian rodent species. To achieve this, we attempt to collate all records of the condition in Australia, both contemporary and historic, using three distinct methods: 1. An examination of historic records by searching a national, digitized newspaper database, and auditing museum collections.

A survey of contemporary ecologists and naturalists, requesting
albino rodent records and a summary of their rodent trapping data to better understand the frequency of the condition.
3. A camera trap survey of a population that is known to produce albino individuals on occasion (rakali on Barrow Island) to better understand the frequency of the condition at that location.
Notably, the patterns of albinism inheritance were not investigated as part of this study.

| Historic records survey
To collate historic records of albino rodents in Australia, we first completed a search of historical (gray literature) records on the Trove digitized newspaper database (https://trove.nla.gov.au/); a freely available, comprehensive digital collection of Australian newspaper articles, gazettes, and other resources dating back to 1762. We searched Trove on the May 24, 2021, using the search terms 'albin rodent', 'albin rat', and 'albin mouse'. These search terms returned 224 articles, of which 200 (89.29%) were removed after screening as they were either duplicates or fell outside the scope of our search (e.g., records of captive rodents, records from outside Australia; Figure A1).
We then audited seven Australian State and Territory museum collections (Australian Museum, Australian National Wildlife Collection, Museum and Art Gallery of the Northern Territory, Museums Victoria, South Australian Museum, Tasmanian Museum and Art Gallery, and Western Australian Museum) for albino specimens with the assistance of mammal curators or collection managers from each institution. They searched their respective institution's collections database for any mention of the word 'albino' attached to native murid specimen records and visually inspected collections for any abnormally pale rodent specimens.
Notably, the collection at the Queensland Museum was inaccessible for the duration of our survey; therefore, this collection was not audited.
There are several large collections of Australian rodent specimens housed in international museums. We searched international museum online databases (American Museum of Natural History National Museum of Natural History) for records of Australian rodents with albinism but did not identify any. Some online databases lacked a notes field (AMNH, MVZ), so while Australian rodent specimens were found, there was no scope for identifying albinism if it were present. We also contacted mammalogy curators, collection managers, or research associates at several of these museums -no respondents could recall any relevant specimens within their collections, and visual inspection of the MVZ collection returned no albinos.

| Contemporary ecologist and naturalist survey
We contacted 69 ecologists and naturalists with extensive experience conducting small mammal trapping surveys in Australia and asked whether they had any contemporary records of albino rodents. If they had recorded an albino, we asked for the year, month, and location of the detection, as well as the species, sex, and weight of the animal. To better understand the frequency with which albino individuals are detected, we also requested a summary of their rodent trapping data. Specifically, we asked for location (region and state), species, sample period (years), and sample size (i.e., the number of individuals captured during the sample period). We received responses regarding albino records from 57 ecologists and naturalists and trapping summaries from 23 ecologists and naturalists. In total, 77 species-specific trapping summaries were provided (some ecologists provided summaries for more than one species) representing 30 species (28 native, 2 non-native). Sample sizes for each species were combined, and we estimated the frequency of albinism only for those species with adequate sample sizes (≥1000 individuals) by dividing the number of albino individuals by the sample size. Notably, some of the larger sample sizes provided were estimated to the nearest hundred (Table A1). The complete trapping summary is available in the Appendix (Table A1). Importantly, we acknowledge that this survey of contemporary ecologists and naturalists, while extensive, was neither systematic nor exhaustive; by virtue of the scale of the task, there remain ecologists that we have not consulted and datasets we have not accessed. As such, there may be additional recent albino rodent records that are not included here.

| Barrow Island camera survey
The current population size of rakali on Barrow Island is not wellknown, but previous estimates have indicated that there may be approximately 150 individual rakali on the island (Bettink, 2016).
To better understand the frequency of albinism in this population, we conducted a camera trap survey across 36 sites on the island Covid-19 restricted visits to the island. Cameras sometimes failed due to heat, salt spray, cyclones, as well as "evisceration" of batteries by white-bellied sea eagles (Haliaeetus leucogaster). At each site, cameras were attached to a 1.2 m picket on a 40 cm right angle bracket, facing the ground. As fishes comprise a large part of the diet of rakali, we used a perforated tin of sardines as a scent lure, secured at the base of each stake. Cameras were set to record five images per trigger event at moderate sensitivity, with no delay between possible trigger events. Each photo sequence was treated as a single point in time, and a detection event was defined as a set of images separated by at least 15 min. Images were processed and rakali were identified by E. Sanders.

| Historic records survey
Our search of the Trove digitized newspaper database revealed 24 records of free-ranging albino rodents in Australia. Of these, 16 were records of unidentified species (Table A2), five were records of invasive species, and three were records of native species (Table 1).
The records of native species comprised one rakali from Victoria (recorded in 1937) and two long-haired rats (R. villosissimus) from Queensland (recorded in 1940 and 1951; Table 1). Of the non-native species, there were three records of the brown rat and two of the house mouse (Table 1).
Auditing of museum collections returned two records of wildcaught native albino or 'part albino' rodent specimens (Table 1) Wales). The giant white-tailed rat specimen has been lost; remaining notes label the specimen as 'albino' with an estimated collection date pre-1900. The canefield rat was a skin specimen, collected from a sugar mill in 1939; it was labeled as 'semi-albino', but appears to have no pigmentation in the skin or fur except a faint pale gray at the base of the dorsal hairs (pers. comm. Sandy Ingleby; Figure 2). The faint colouration and the absence of eyes (by nature of being a dry specimen) mean leucism cannot be ruled out. In addition, there were two records of captive-born long-haired rats from the South Australian Museum (Table 1). Of these, only one (spirit) specimen remains; it is a confirmed true albino with red eyes (Figure 2). There are, however, no data available on the founder source location or generation of the captive-born animals.

| Contemporary ecologist/naturalist survey
We collated approximately 53,159 contemporary records of livetrapped, individual free-ranging rodents in Australia; representing 30 species from 10 genera (Table A2). There were 16 records of free-ranging albino rodents (dating from 1980-2021) representing six species native to Australia and one non-native species (Table 1; Figure 3). The most common species in which albinism was recorded was the rakali with six detections (all from Barrow Island) and the bush rat (Rattus fuscipes) with four detections, followed by the longhaired rat with two detections, and the heath mouse (Pseudomys shortridgei), ash-gray mouse (P. albocinereus), desert mouse (P. desertor), and the non-native house mouse each with one detection (Table 1). Most animals were live-trapped, except for one bush rat that was recorded on a white-flash camera trap, and three rakali that were opportunistically observed during nocturnal fauna surveys (Table 1; Figure 3). The frequency of albinism was calculated for the bush rat (0.03%), long-haired rat (0.06%), desert mouse (0.08%), heath mouse (0.09%), and the non-native house mouse (0.01%). The frequency of albinism for the rakali and ash-gray mouse were not calculated, as these species had sample sizes <1000 (Table A2).
The sex ratio of albino rodents (where data were available) was equal, with six females and six males. Body weight information was available for 10 records, and the majority of individuals were relatively lightweight (Menkhorst & Knight, 2001), although no obvious signs of poor body condition or high parasite load were reported for these animals. No other physical abnormalities were reported.

| Barrow Island camera survey
We recorded a total of 285 rakali detections on Barrow Island, with rakali recorded at 34 of the 36 camera sites. There were seven detections of albino rakali ( Figure 4) from a total of three sites (RA01, RA02, and RA36). Sites RA01 are RA02 were approximately 1 km apart, and while it is possible for a rakali to traverse this distance and be detected at both sites, at least two individuals could be differentiated in the camera trap images (one individual had a distinctive tail kink). Site RA36 is over 5 km from the RA01 and RA02 sites (Figure 1), and this distance is longer than overland traverses previously recorded in the species (Gardner & Serena, 1995;Harris, 1978;Vernes, 1998). Therefore, it is likely that a minimum of three albino rakali were detected on Barrow Island (Table 1), and that the frequency of albinism in this population was at least 2%, assuming a population size of 150 individuals (Bettink, 2016).

| DISCUSS ION
Our surveys uncovered 23 native, free-ranging albino murid rodent records from across Australia. These records represent eight spe-

Contemporary Chris Dickman
Note: There were 31 records of albino rodents identified from our surveys, including eight records from the gray literature survey (three native, five non-native), four records from the museum survey (two wild-born, two captive-born), 16 records from the contemporary survey (15 native, one non-native), and three records from the camera trap survey on Barrow Island. Non-native species are denoted by an asterisk next to the species name. Month, region, and weight of specimen record are provided in parentheses where data were available. The complete contemporary survey list, which includes references and rodent species for which no albinos were recorded, can be found in the Appendix (Table A1)

TA B L E 1 (Continued)
endemics (the canefield rat, long-haired rat, and bush rat). To our knowledge, this represents the first occasion that records of albinism in free-ranging rodents native to Australia have been recorded in the published literature.
Records of albinism in free-ranging rodents are rare; a review by Romero et al. (2018) found that albino specimens have been reported in just 64 of 2683 species in the order Rodentia (sensu Upham et al., 2022), with no records from Australian species.
Since 2018, four more rodent species have been added to that list (Dalapicolla et al., 2020;Nations et al., 2021;Stumpp et al., 2019;van der Geer, 2019). The addition of the eight Australian species reported in this study represents a considerable (11.8%) increase in the number of rodent species, globally, with albinism recorded, and nearly doubles the number of murid rodent species from 11 to 19 (1.3% to 2.2%). We also identified seven records of albinism in two of Australia's four invasive rodent species, the house mouse and brown rat; however, albinism has been previously reported in these species (see Romero et al., 2018).
In line with Romero et al. (2018), the results from our contemporary survey also emphasize the rarity of the condition in rodents, with our 16 records (representing six native species and one nonnative species) arising from a sample of over 53,000 individuals (representing 30 species). We are assuming, however, that the encounter with an albino animal would be both obvious enough for most F I G U R E 2 Images of two preserved albino rodent bodies identified from our survey of Australian museums: (a) dorsal image of a canefield rat (Rattus sordidus), which was labeled as 'semi-albino' from the Australian Museum (New South Wales) but appears to have no pigmentation in the skin or fur except a faint pale gray at the base of the dorsal hairs (pers. comm. Sandy Ingleby; image credit Sandy Ingleby); (b) ventral image of the same canefield rat (image credit Sandy Ingleby); (c) image of a captive-born long-haired rat (R. villosissimus) from the South Australian Museum. No data were available on the founder source location or generation of the captive-born animals (image credit David Stemmer). The frequency of albinism can, however, increase under certain conditions, such as inbreeding among small isolated populations or between closely related individuals (Caro, 2009). The rakali population on Barrow Island has been isolated for at least 8000 years and, as a result, likely has little genetic diversity and exhibits the effects of genetic drift and inbreeding depression (Bettink, 2016).

F I G U R E 3
Our survey of contemporary ecologists and naturalists identified six albino rakali records from Barrow Island, and our camera trap survey suggests that there were at least three albino individuals persisting on the island probably simultaneously (three records within 1 month). Our estimate that at least 1 in 50 individuals (2%) of the Barrow Island rakali population are albino is considerably higher than our other estimates from the contemporary survey, which ranged from 1 in ~1100 to 1 in 10,000 ( Excluding the Barrow Island Hydromys, eight of the 14 records of albinism in Australian rodents were from arid and semi-arid species (ash gray mouse, desert mouse, long-haired rat) which exhibit an irruptive (boom-bust) population cycle (Dickman et al., 1999;Greenville et al., 2012;Madsen & Shine, 1999). These dramatic fluctuations typically occur in arid and semi-arid environments in response to pulses in primary productivity catalyzed by rainfall events, which occur unreliably in these environments (Dickman et al., 1999;Greenville et al., 2012;Madsen & Shine, 1999). Significant rainfall events can facilitate a pulse of productivity (Whitford & Duval, 2019) after which rodent populations often erupt-a period known as the 'boom' phase (Dickman et al., 1999(Dickman et al., , 2010Madsen & Shine, 1999;Plomley, 1972). This intense response to rainfall is driven by highreproductive rates, increased survival, and the potential for females to birth multiple litters in a year. In these instances, greater resource F I G U R E 4 Photographs of free-ranging rakali from the camera trap survey on Barrow Island, Western Australia, undertaken from October 2019-January 2021: (a) an image of a non-albino rakali from site RA36, (b) an image of an albino rakali from site RA36, (c) an image of a non-albino rakali from site RA02, and (d) an image of an albino rakali from site RA02.
availability and recruitment may increase both the likelihood of albino offspring being produced (higher number of births rather than an increase in proportion of albino births) and the likelihood of their survival to adulthood by improving access to food and shelter resources, hence reducing competition and predation pressures. Our contemporary records of albinism in the desert mouse and longhaired rat were made after prolonged wet periods when populations of these species were high (Dickman et al., 2014;Greenville et al., 2013Greenville et al., , 2016; however, an in-depth investigation into the influence of rainfall on the frequency of albinism detections in Australian rodents was considered beyond the scope of this research. The sex ratio reported in this study was equal; rakali, bush rats, and long-haired rats-which account for the majority of those records-often exhibit even sex ratios (Predavec & Dickman, 1994;Press, 1987;Smart et al., 2011;Speldewinde et al., 2013;Valentine et al., 2009), although populations of long-haired rats can skew towards either males or females (Carstairs, 1976;Predavec & Dickman, 1994). Furthermore, a survey of rakali by Bettink (2016) identified a male-skewed sex bias on Barrow Island, albeit from a relatively small sample (n = 11). Most individuals with bodyweight data were relatively lightweight (Menkhorst & Knight, 2001); however, due to the small sample size of albino individuals, we were unable to infer any potential influence of albinism on sex ratio or body condition in this study, although instances of poor body condition were not reported, and we are not aware of albinism influencing the sex ratio of free-ranging mammal populations. Investigation (supporting); methodology (supporting); project administration (supporting); visualization (supporting); writing -original draft (supporting); writing -review and editing (supporting).

ACK N OWLED G M ENTS
We acknowledge the Wurundjeri People as the Traditional

DJW was supported by a Deakin University Postgraduate Research
Scholarship. No additional external funding was provided for this research.